Gain or Loss? Evidence for Legume Predisposition to Symbiotic Interactions with Rhizobia via Loss of Pathogen-Resistance-Related Gene Families
Nodulation is a hallmark yet non-universal characteristic of legumes. It is unknown whether the mechanisms underlying nitrogen-fixing symbioses evolved within legumes and the broader nitrogen-fixing clade (NFC) repeatedly de novo or based on common ancestral pathways. Ten new transcriptomes represen...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-12-01
|
| Series: | International Journal of Molecular Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1422-0067/23/24/16003 |
| _version_ | 1797457231942254592 |
|---|---|
| author | Katarzyna B. Czyż Candy M. Taylor Michał Kawaliło Grzegorz Koczyk |
| author_facet | Katarzyna B. Czyż Candy M. Taylor Michał Kawaliło Grzegorz Koczyk |
| author_sort | Katarzyna B. Czyż |
| collection | DOAJ |
| description | Nodulation is a hallmark yet non-universal characteristic of legumes. It is unknown whether the mechanisms underlying nitrogen-fixing symbioses evolved within legumes and the broader nitrogen-fixing clade (NFC) repeatedly de novo or based on common ancestral pathways. Ten new transcriptomes representing members from the Cercidoideae and Caesalpinioideae subfamilies were supplemented with published omics data from 65 angiosperms, to investigate how gene content correlates with nodulation capacity within Fabaceae and the NFC. Orthogroup analysis categorized annotated genes into 64150 orthogroups, of which 19 were significantly differentially represented between nodulating versus non-nodulating NFC species and were most commonly absent in nodulating taxa. The distribution of six over-represented orthogroups within Viridiplantae representatives suggested that genomic evolution events causing gene family expansions, including whole-genome duplications (WGDs), were unlikely to have facilitated the development of stable symbioses within Fabaceae as a whole. Instead, an absence of representation of 13 orthogroups indicated that losses of genes involved in trichome development, defense and wounding responses were strongly associated with rhizobial symbiosis in legumes. This finding provides novel evidence of a lineage-specific predisposition for the evolution and/or stabilization of nodulation in Fabaceae, in which a loss of pathogen resistance genes may have allowed for stable mutualistic interactions with rhizobia. |
| first_indexed | 2024-03-09T16:19:15Z |
| format | Article |
| id | doaj.art-eb6792904a3848b0b13056e2599bf4fa |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-09T16:19:15Z |
| publishDate | 2022-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-eb6792904a3848b0b13056e2599bf4fa2023-11-24T15:31:13ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-12-0123241600310.3390/ijms232416003Gain or Loss? Evidence for Legume Predisposition to Symbiotic Interactions with Rhizobia via Loss of Pathogen-Resistance-Related Gene FamiliesKatarzyna B. Czyż0Candy M. Taylor1Michał Kawaliło2Grzegorz Koczyk3Biometry and Bioinformatics Team, Institute of Plant Genetics Polish Academy of Science, 60-479 Poznań, PolandSchool of Agriculture and Environment, The University of Western Australia, Perth, WA 6009, AustraliaBiometry and Bioinformatics Team, Institute of Plant Genetics Polish Academy of Science, 60-479 Poznań, PolandBiometry and Bioinformatics Team, Institute of Plant Genetics Polish Academy of Science, 60-479 Poznań, PolandNodulation is a hallmark yet non-universal characteristic of legumes. It is unknown whether the mechanisms underlying nitrogen-fixing symbioses evolved within legumes and the broader nitrogen-fixing clade (NFC) repeatedly de novo or based on common ancestral pathways. Ten new transcriptomes representing members from the Cercidoideae and Caesalpinioideae subfamilies were supplemented with published omics data from 65 angiosperms, to investigate how gene content correlates with nodulation capacity within Fabaceae and the NFC. Orthogroup analysis categorized annotated genes into 64150 orthogroups, of which 19 were significantly differentially represented between nodulating versus non-nodulating NFC species and were most commonly absent in nodulating taxa. The distribution of six over-represented orthogroups within Viridiplantae representatives suggested that genomic evolution events causing gene family expansions, including whole-genome duplications (WGDs), were unlikely to have facilitated the development of stable symbioses within Fabaceae as a whole. Instead, an absence of representation of 13 orthogroups indicated that losses of genes involved in trichome development, defense and wounding responses were strongly associated with rhizobial symbiosis in legumes. This finding provides novel evidence of a lineage-specific predisposition for the evolution and/or stabilization of nodulation in Fabaceae, in which a loss of pathogen resistance genes may have allowed for stable mutualistic interactions with rhizobia.https://www.mdpi.com/1422-0067/23/24/16003Fabaceaenodulationnitrogen-fixing symbiosisgene losscomparative genomicsplant–pathogen interaction genes |
| spellingShingle | Katarzyna B. Czyż Candy M. Taylor Michał Kawaliło Grzegorz Koczyk Gain or Loss? Evidence for Legume Predisposition to Symbiotic Interactions with Rhizobia via Loss of Pathogen-Resistance-Related Gene Families International Journal of Molecular Sciences Fabaceae nodulation nitrogen-fixing symbiosis gene loss comparative genomics plant–pathogen interaction genes |
| title | Gain or Loss? Evidence for Legume Predisposition to Symbiotic Interactions with Rhizobia via Loss of Pathogen-Resistance-Related Gene Families |
| title_full | Gain or Loss? Evidence for Legume Predisposition to Symbiotic Interactions with Rhizobia via Loss of Pathogen-Resistance-Related Gene Families |
| title_fullStr | Gain or Loss? Evidence for Legume Predisposition to Symbiotic Interactions with Rhizobia via Loss of Pathogen-Resistance-Related Gene Families |
| title_full_unstemmed | Gain or Loss? Evidence for Legume Predisposition to Symbiotic Interactions with Rhizobia via Loss of Pathogen-Resistance-Related Gene Families |
| title_short | Gain or Loss? Evidence for Legume Predisposition to Symbiotic Interactions with Rhizobia via Loss of Pathogen-Resistance-Related Gene Families |
| title_sort | gain or loss evidence for legume predisposition to symbiotic interactions with rhizobia via loss of pathogen resistance related gene families |
| topic | Fabaceae nodulation nitrogen-fixing symbiosis gene loss comparative genomics plant–pathogen interaction genes |
| url | https://www.mdpi.com/1422-0067/23/24/16003 |
| work_keys_str_mv | AT katarzynabczyz gainorlossevidenceforlegumepredispositiontosymbioticinteractionswithrhizobiavialossofpathogenresistancerelatedgenefamilies AT candymtaylor gainorlossevidenceforlegumepredispositiontosymbioticinteractionswithrhizobiavialossofpathogenresistancerelatedgenefamilies AT michałkawaliło gainorlossevidenceforlegumepredispositiontosymbioticinteractionswithrhizobiavialossofpathogenresistancerelatedgenefamilies AT grzegorzkoczyk gainorlossevidenceforlegumepredispositiontosymbioticinteractionswithrhizobiavialossofpathogenresistancerelatedgenefamilies |